The territory is putting rights to more than 160,000 hectares in the central Mackenzie Valley on the block.
The devolution agreement with the federal government took effect last April.
"It's a positive step forward for us, and a bit of a maturation for us as we move into our new responsibilities as a government," Dave Ramsay, industry, tourism and investment minister, said from Ottawa.
Ramsay acknowledged the oil-price crash may not be the best time to put new rights on the market, but he added the response to the offering has been positive.
"We still have a resource in the central Mackenzie that folks are interested in."
Ramsay said the auction's rules are the same as when it was run by the federal Indian Affairs Department.
But this time all the revenues from the auction will go to the Northwest Territories and not to Ottawa.
Ramsay said last year's royalties from oil and gas reached $120 million, which was shared by the federal, territorial and aboriginal governments.
The territory is considered to have large undeveloped reserves of oil and gas. By some estimates, it could hold up to 37 per cent of Canada’s marketable light crude oil resources and 35 per cent of its marketable natural gas resources.
The closing date for the rights auction is June 2.